Abstract
Parasites are one of the strongest selective agents in nature. They select for hosts that evolve counter‐adaptive strategies to cope with infection. Helminth parasites are special because they can modulate their hosts’ immune responses. This phenomenon is important in epidemiological contexts, where coinfections may be affected. How different types of hosts and helminths interact with each other is insufficiently investigated. We used the three‐spined stickleback (Gasterosteus aculeatus) – Schistocephalus solidus model to study mechanisms and temporal components of helminth immune modulation. Sticklebacks from two contrasting populations with either high resistance (HR) or low resistance (LR) against S. solidus, were individually exposed to S. solidus strains with characteristically high growth (HG) or low growth (LG) in G. aculeatus. We determined the susceptibility to another parasite, the eye fluke Diplostomum pseudospathaceum, and the expression of 23 key immune genes at three time points after S. solidus infection. D. pseudospathaceum infection rates and the gene expression responses depended on host and S. solidus type and changed over time. Whereas the effect of S. solidus type was not significant after three weeks, T regulatory responses and complement components were upregulated at later time points if hosts were infected with HG S. solidus. HR hosts showed a well orchestrated immune response, which was absent in LR hosts. Our results emphasize the role of regulatory T cells and the timing of specific immune responses during helminth infections. This study elucidates the importance to consider different coevolutionary trajectories and ecologies when studying host‐parasite interactions.
Highlights
The evolution of species and species interactions are shaped through a complex web of abiotic and biotic factors (Betts, Rafaluk, & King, 2016; Maizels & Nussey, 2013; Schulenburg, Kurtz, Moret, & Siva‐Jothy, 2009; Sheldon & Verhulst, 1996)
Post hoc comparisons of the effects of parasite type over time and with regard to host type showed that three weeks after S. solidus infection, low resistance (LR) hosts had more D. pseudospathaceum meta‐ cercariae in their eyes if infected with high growth (HG) S. solidus or sham‐exposed, than those infected with low growth (LG) S. solidus; in week 6, D. pseudospatha‐ ceum numbers in LR fish were highest if hosts were infected with HG S. solidus and lowest in controls; in high resistance (HR) hosts, D. pseudospatha‐ ceum infection rates were significantly higher in HG infected hosts (a)
Using controlled experimental helminth infections of three‐spined sticklebacks, we found that proinflammatory, complement and T regulatory pathways are upregulated in chronic infections with a high growth (HG) Schistocephalus solidus type after the cestode reached its reproductive weight
Summary
The evolution of species and species interactions are shaped through a complex web of abiotic and biotic factors (Betts, Rafaluk, & King, 2016; Maizels & Nussey, 2013; Schulenburg, Kurtz, Moret, & Siva‐Jothy, 2009; Sheldon & Verhulst, 1996). Tregs are considered to be key controllers of im‐ mune system homeostasis and expand upon longstanding helminth infections Modulation of these cells may protect from immunopa‐ thology and ensure the persistence of the parasite within the host. The stickle‐ back's immune system is principally able to eliminate S. solidus up to 17 days post infection, adaptive immune responses might be active after 2–3 weeks, and head kidney leucocyte respiratory burst poten‐ tial (an estimate for innate immune activation) peaks after 7–9 weeks (Barber & Scharsack, 2010; Scharsack et al, 2007). S. solidus’ effect on stickleback immune gene expression was studied in S. solidus infected and coinfected hosts (Figure 1)
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